The hyperfibrinolytic state of mice with combined thrombin-activatable fibrinolysis inhibitor (TAFI) and plasminogen activator inhibitor-1 gene deficiency is critically dependent on TAFI deficiency

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 12, 2012, Pages 2555-2562

  Vercauteren, E ^a   Peeters, M ^a   Hoylaerts, M F ^b   Lijnen, H R ^b   Meijers, J C M ^c   Declerck, P J ^a   Gils, A ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Fibrinolysis; Gene deficiency; Mouse thrombosis models; Plasminogen activator inhibitor 1; Thrombin activatable fibrinolysis inhibitor

Indexed keywords

PLASMINOGEN ACTIVATOR INHIBITOR 1; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLEEDING TIME; BLOOD SAMPLING; CONTROLLED STUDY; FEMALE; FERTILE PERIOD; GENE; IN VIVO STUDY; MALE; MATING; MOUSE; NONHUMAN; PHENOTYPE; PLASMINOGEN ACTIVATOR INHIBITOR 1 GENE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; THROMBIN ACTIVATABLE FIBRINOLYSIS INHIBITOR GENE; THROMBOEMBOLISM;

ANIMALS; BASE SEQUENCE; CARBOXYPEPTIDASE U; DNA PRIMERS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMINOGEN ACTIVATOR INHIBITOR 1;

EID: 84871057895     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/jth.12036     Document Type: Article

References (43)

1. Bajzar L, Morser J, Nesheim M. TAFI, or plasma procarboxypeptidase B, couples the coagulation and fibrinolytic cascades through the thrombin-thrombomodulin complex. J Biol Chem 1996; 271: 16603-8.
2. Rijken DC, Lijnen HR. New insights into the molecular mechanisms of the fibrinolytic system. J Thromb Haemost 2009; 7: 4-13.
3. Mosnier LO, Buijtenhuijs P, Marx PF, Meijers JCM, Bouma BN. Identification of thrombin activatable fibrinolysis inhibitor (TAFI) in human platelets. Blood 2003; 101: 4844-6.
4. Andreasen PA, Riccio A, Welinder KG, Douglas R, Sartorio R, Nielsen LS, Oppenheimer C, Blasi F, Dano K. Plasminogen activator inhibitor type-1 - reactive center and amino-terminal heterogeneity determined by protein and cDNA sequencing. FEBS Lett 1986; 209: 213-18.
5. Booth NA, Simpson AJ, Croll A, Bennett B, Macgregor IR. Plasminogen activator inhibitor (PAI-1) in plasma and platelets. Br J Haematol 1988; 70: 327-33.
6. Brogren H, Wallmark K, Deinum J, Karlsson L, Jern S. Platelets retain high levels of active plasminogen activator inhibitor 1. PLoS One 2011; 6: e26762.
7. Boulaftali Y, Ho-Tin-Noe B, Pena A, Loyau S, Venisse L, Francois D, Richard B, Arocas V, Collet J-P, Jandrot-Perrus M, Bouton M-C. Platelet protease nexin-1, a serpin that strongly influences fibrinolysis and thrombolysis. Circulation 2011; 123: 1326-34.
8. van De Craen B, Declerck PJ, Gils A. The biochemistry, physiology and pathological roles of PAI-1 and the requirements for PAI-1 inhibition in vivo. Thromb Res 2012; 130: 576-85.
9. Mullertz S, Clemmensen I. Primary inhibitor of plasmin in human plasma. Biochem J 1976; 159: 545-53.
10. te Velde EA, Wagenaar GTM, Reijerkerk A, Roose-Girma M, Rinkes I, Voest EE, Bouma BN, Gebbink M, Meijers JCM. Impaired healing of cutaneous wounds and colonic anastomoses in mice lacking thrombin-activatable fibrinolysis inhibitor. J Thromb Haemost 2003; 1: 2087-96.
11. Morser J, Gabazza EC, Myles T, Leung LLK. What has been learnt from the thrombin-activatable fibrinolysis inhibitor-deficient mouse? J Thromb Haemost 2010; 8: 868-76.
12. Carmeliet P, Kieckens L, Schoonjans L, Ream B, Vannuffelen A, Prendergast G, Cole M, Bronson R, Collen D, Mulligan RC. Plasminogen activator inhibitor-1 gene deficient mice. 1. Generation by homologous recombination and characterization. J Clin Invest 1993; 92: 2746-55.
13. Declerck PJ, Gils A, De Taeye B. Use of mouse models to study plasminogen activator inhibitor-1. Methods Enzymol Biol Serpin 2011; 499: 77-104.
14. Lijnen HR, Okada K, Matsuo O, Collen D, Dewerchin M. alpha(2)-Antiplasmin gene deficiency in mice is associated with enhanced fibrinolytic potential without overt bleeding. Blood 1999; 93: 2274-81.
15. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Berns A. Simplified mammalian DNA isolation procedure. Nucleic Acids Res 1991; 19: 4293.
16. Hillmayer K, Brouwers E, Leon-Tamariz F, Meijers JCM, Marx PF, Declerck PJ, Gils A. Development of sandwich-type ELISAs for the quantification of rat and murine thrombin activatable fibrinolysis inhibitor in plasma. J Thromb Haemost 2008; 6: 132-8.
17. Kawasaki T, Dewerchin M, Lijnen HR, Vermylen J, Hoylaerts MF. Vascular release of plasminogen activator inhibitor-1 impairs fibrinolysis during acute arterial thrombosis in mice. Blood 2000; 96: 153-60.
18. Denis C, Methia N, Frenette PS, Rayburn H, Ullman-Cullere M, Hynes RO, Wagner DD. A mouse model of severe von Willebrand disease: defects in hemostasis and thrombosis. Proc Natl Acad Sci USA 1998; 95: 9524-9.
19. De Meyer SF, Vandeputte N, Pareyn I, Petrus I, Lenting PJ, Chuah MKL, VandenDriessche T, Deckmyn H, Vanhoorelbeke K. Restoration of plasma von Willebrand factor deficiency is sufficient to correct thrombus formation after gene therapy for severe von Willebrand disease. Arterioscler Thromb Vasc Biol 2008; 28: 1621-6.
20. Vercauteren E, Emmerechts J, Peeters M, Hoylaerts MF, Declerck PJ, Gils A. Evaluation of the profibrinolytic properties of an anti-TAFI monoclonal antibody in a mouse thromboembolism model. Blood 2011; 117: 4615-22.
21. Carmeliet P, Stassen JM, Schoonjans L, Ream B, Vandenoord JJ, Demol M, Mulligan RC, Collen D. Plasminogen activator inhibitor-1 gene deficient mice. 2. Effects on hemostasis, thrombosis, and thrombolysis. J Clin Invest 1993; 92: 2756-60.
22. Greene TK, Schiviz A, Hoellriegl W, Poncz M, Muchitsch EM. Sci Standardization Comm I. Towards a standardization of the murine tail bleeding model. J Thromb Haemost 2010; 8: 2820-2.
23. Nagashima M, Yin ZF, Broze GJ, Morser J. Thrombin-activatable fibrinolysis inhibitor (TAFI) deficient mice. Front Biosci 2002; 7: D556-68.
24. Swaisgood CM, Schmitt D, Eaton D, Plow EF. In vivo regulation of plasminogen function by plasma carboxypeptidase B. J Clin Invest 2002; 110: 1275-82.
25. Broze GJ, Yin ZF, Lasky N. A tail vein bleeding time model and delayed bleeding in hemophiliac mice. Thromb Haemost 2001; 85: 747-8.
26. Wang XK, Smith PL, Hsu MY, Tamasi JA, Bird E, Schumacher WA. Deficiency in thrombin-activatable fibrinolysis inhibitor (TAFI) protected mice from ferric chloride-induced vena cava thrombosis. J Thromb Thrombolysis 2007; 23: 41-9.
27. Nagashima M, Yin ZF, Zhao L, White K, Zhu YH, Lasky N, Halks-Miller M, Broze GJ, Fay WP, Morser J. Thrombin-activatable fibrinolysis inhibitor (TAFI) deficiency is compatible with murine life. J Clin Invest 2002; 109: 101-10.
28. Mao SS, Holahan MA, Bailey C, Wu GX, Colussi D, Carroll SS, Cook JJ. Demonstration of enhanced endogenous fibrinolysis in thrombin activatable fibrinolysis inhibitor-deficient mice. Blood Coagul Fibrinolysis 2005; 16: 407-15.
29. Farrehi PM, Ozaki CK, Carmeliet P, Fay WP. Regulation of arterial thrombolysis by plasminogen activator inhibitor-1 in mice. Circulation 1998; 97: 1002-8.
30. Fay WP, Parker AC, Ansari MN, Zheng XX, Ginsburg D. Vitronectin inhibits the thrombotic response to arterial injury in mice. Blood 1999; 93: 1825-30.
31. Konstantinides S, Schafer K, Thinnes T, Loskutoff DJ. Plasminogen activator inhibitor-1 and its cofactor vitronectin stabilize arterial thrombi after vascular injury in mice. Circulation 2001; 103: 576-83.
32. Eitzman DT, Westrick RJ, Nabel EG, Ginsburg D. Plasminogen activator inhibitor-1 and vitronectin promote vascular thrombosis in mice. Blood 2000; 95: 577-80.
33. Matsuno H, Kozawa O, Niwa M, Ueshima S, Matsuo O, Collen D, Uematsu T. Differential role of components of the fibrinolytic system in the formation and removal of thrombus induced by endothelial injury. Thromb Haemost 1999; 81: 601-4.
34. Schleef RR, Higgins DL, Pillemer E, Levitt LJ. Bleeding diathesis due to decreased functional activity of type-1 plasminogen activator inhibitor. J Clin Invest 1989; 83: 1747-52.
35. Dieval J, Nguyen G, Gross S, Delobel J, Kruithof EKO. A lifelong bleeding disorder associated with a deficiency of plasminogen activator inhibitor type-1. Blood 1991; 77: 528-32.
36. Lee MH, Vosburgh E, Anderson K, McDonagh J. Deficiency of plasma plasminogen activator inhibitor-1 results in hyperfibrinolytic bleeding. Blood 1993; 81: 2357-62.
37. Fay WP, Parker AC, Condrey LR, Shapiro AD. Human plasminogen activator inhibitor-1 (PAI-1) deficiency: characterization of a large kindred with a null mutation in the PAI-1 gene. Blood 1997; 90: 204-8.
38. Minowa H, Takahashi Y, Tanaka T, Naganuma K, Ida S, Maki I, Yoshioka A. Four cases of bleeding diathesis in children due to congenital plasminogen activator inhibitor-1 deficiency. Haemostasis 1999; 29: 286-91.
39. Dewilde M, van De Craen B, Compernolle G, Madsen JB, Strelkov S, Gils A, Declerck PJ. Subtle structural differences between human and mouse PAI-1 reveal the basis for biochemical differences. J Struct Biol 2010; 171: 95-101.
40. Lijnen HR, Vanhoef B, Beelen V, Collen D. Characterization of the murine plasma fibrinolytic system. Eur J Biochem 1994; 224: 863-71.
41. Declerck PJ, Verstreken M, Collen D. Immunoassay of murine t-PA, u-PA and PAI-1 using monoclonal antibodies raised in gene inactivated mice. Thromb Haemost 1995; 74: 1305-9.
42. Zhu YH, Carmeliet P, Fay WP. Plasminogen activator inhibitor-1 is a major determinant of arterial thrombolysis resistance. Circulation 1999; 99: 3050-5.
43. Dewerchin M, Collen D, Lijnen HR. Enhanced fibrinolytic potential in mice with combined homozygous deficiency of alpha(2)-antiplasmin and PAI-1. Thromb Haemost 2001; 86: 640-6.